Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2

November 7, 2000
97 (24) 13430-13435

Abstract

Net photosynthesis (Pn) is inhibited by moderate heat stress. To elucidate the mechanism of inhibition, we examined the effects of temperature on gas exchange and ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activation in cotton and tobacco leaves and compared the responses to those of the isolated enzymes. Depending on the CO2 concentration, Pn decreased when temperatures exceeded 35–40°C. This response was inconsistent with the response predicted from the properties of fully activated Rubisco. Rubisco deactivated in leaves when temperature was increased and also in response to high CO2 or low O2. The decrease in Rubisco activation occurred when leaf temperatures exceeded 35°C, whereas the activities of isolated activase and Rubisco were highest at 42°C and >50°C, respectively. In the absence of activase, isolated Rubisco deactivated under catalytic conditions and the rate of deactivation increased with temperature but not with CO2. The ability of activase to maintain or promote Rubisco activation in vitro also decreased with temperature but was not affected by CO2. Increasing the activase/Rubisco ratio reduced Rubisco deactivation at higher temperatures. The results indicate that, as temperature increases, the rate of Rubisco deactivation exceeds the capacity of activase to promote activation. The decrease in Rubisco activation that occurred in leaves at high CO2 was not caused by a faster rate of deactivation, but by reduced activase activity possibly in response to unfavorable ATP/ADP ratios. When adjustments were made for changes in activation state, the kinetic properties of Rubisco predicted the response of Pn at high temperature and CO2.

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References

1
C Rosenweig, D Hillel Climate Change and the Global Harvest: Potential Impacts of the Greenhouse Effect on Agriculture (Oxford Univ. Press, Oxford, 1998).
2
J A Berry, O Björkman Annu Rev Plant Physiol 31, 491–543 (1980).
3
S-B Ku, G E Edwards Plant Physiol 59, 986–990 (1977).
4
R K Monson, M A Stidham, G J Williams, G E Edwards Plant Physiol 69, 921–928 (1982).
5
D B Jordan, W L Ogren Planta 161, 308–313 (1984).
6
R F Sage, T D Sharkey Plant Physiol 84, 658–664 (1987).
7
G D Farquhar, S von Caemmerer, J A Berry Planta 149, 178–190 (1980).
8
T D Sharkey Bot Rev 51, 53–105 (1985).
9
J T Perchorowicz, D A Raynes, R G Jensen Proc Natl Acad Sci USA 78, 2985–2989 (1981).
10
E Weis Planta 151, 33–39 (1981).
11
E Weis FEBS Lett 129, 197–200 (1981).
12
T D Sharkey, J R Seeman, J A Berry Plant Physiol 81, 788–791 (1986).
13
R F Sage, T D Sharkey, J R Seeman Planta 174, 407–416 (1988).
14
R F Sage, T D Sharkey, J R Seeman Plant Physiol 89, 590–596 (1989).
15
A Makino, T Mae Plant Cell Physiol 40, 999–1006 (1999).
16
J Kobza, G E Edwards Plant Physiol 83, 69–74 (1987).
17
U Feller, S J Crafts-Brandner, M E Salvucci Plant Physiol 116, 539–546 (1998).
18
R D Law, S J Crafts-Brandner Plant Physiol 120, 173–181 (1999).
19
I E Woodrow, M E Kelly, K A Mott Aust J Plant Physiol 23, 141–149 (1996).
20
M R Badger, G H Lorimer J Biol Chem 254, 5599–5601 (1979).
21
D B Jordan, R Chollet J Biol Chem 258, 13752–13758 (1983).
22
T J Andrews Nat Struct Biol 3, 3–7 (1996).
23
A F Neuwald, L Aravind, J L Spouge, E V Koonin Genome Res 9, 27–43 (1999).
24
M E Salvucci, W L Ogren Photosynth Res 47, 1–11 (1996).
25
A R Portis J Exp Bot 46, 1285–1291 (1995).
26
Z Y Wang, A R Portis Plant Physiol 99, 1348–1353 (1992).
27
S P Robinson, A R Portis Arch Biochem Biophys 268, 93–99 (1989).
28
Crafts-Brandner, S. J. & Law, R. D. (2000) Planta, in press.
29
M E Salvucci Arch Biochem Biophys 298, 688–696 (1992).
30
M E Salvucci, R R Klein Arch Biochem Biophys 314, 178–185 (1994).
31
F J van de Loo, M E Salvucci Biochemistry 35, 8143–8148 (1996).
32
N Zhang, A R Portis Proc Natl Acad Sci USA 96, 9438–9443 (1999).
33
W A Laing, W L Ogren, R H Hageman Plant Physiol 54, 678–685 (1974).
34
C J Mate, G S Hudson, S von Caemmerer, J R Evans, T J Andrews Plant Physiol 102, 1119–1128 (1993).
35
J A Bunce Photosynth Res 63, 59–67 (2000).
36
G H Lorimer J Biol Chem 254, 5599–5601 (1979).
37
S J Crafts-Brandner, F J van de Loo, M E Salvucci Plant Physiol 114, 439–444 (1997).
38
P Gardeström, B Wigge Plant Physiol 88, 69–76 (1988).
39
N G Bukhov, C Wiese, S Neimanis, U Heber Photosynth Res 59, 81–93 (1999).

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Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 97 | No. 24
November 21, 2000
PubMed: 11069297

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Submission history

Received: August 24, 2000
Accepted: September 20, 2000
Published online: November 7, 2000
Published in issue: November 21, 2000

Authors

Affiliations

Steven J. Crafts-Brandner*
Western Cotton Research Laboratory, U.S. Department of Agriculture, 4135 East Broadway Road, Phoenix, AZ 85040
Michael E. Salvucci
Western Cotton Research Laboratory, U.S. Department of Agriculture, 4135 East Broadway Road, Phoenix, AZ 85040

Notes

*
To whom reprint requests should be addressed. E-mail: [email protected].
Communicated by William L. Ogren, U.S. Department of Agriculture, Hilton Head Island, SC

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    Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2
    Proceedings of the National Academy of Sciences
    • Vol. 97
    • No. 24
    • pp. 12933-13460

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